Balclutha jafara Webb, 1978

Zahniser, James N., Halbert, Susan E., Moore, Matthew R., Mottern, Jason L. & Beuzelin, Julien M., 2023, Balclutha jafara (Hemiptera: Cicadellidae): integrative identification of a species introduced in the Western Hemisphere, and notes on other Balclutha, Zootaxa 5361 (4), pp. 526-554 : 531-537

Balclutha jafara Webb

Figs. 1–27 , 77–78

Description. Male 2.6–3.1 mm. Female 3.0– 3.5 mm. Color pale yellow to yellow or light greenish; some specimens with additional bright orange or red coloration on posterior half of pronotum, along forewings, on frontoclypeus, on genae below eye, on legs, and/or on dorsal side of abdomen; dorsal and ventral sides of thorax and abdomen usually light, without dark coloration. Forewing mostly hyaline; basal 1/3 between costal margin and R+M and/or R thickened and with opaque yellow or greenish coloration. Head wider than pronotum; crown evenly rounded, not produced; crown texture shagreen. Face relatively broad; genae wide; clypellus slightly expanding toward apex; apex of clypellus nearly straight, not surpassing normal curve of gena. Pronotum surface texture shagreen, with faint transverse depressions. Male pygofer without ventral or ventroapical process; with 8–10 macrosetae arranged in 2 irregular rows along a diagonal from dorsal side (1/3 from base of pygofer) toward posteroventral corner; ventral margin relatively straight, with slight undulations, posteroventrally forming a more or less quadrate angle with posterior margin; posterodorsal lobe with numerous very short setae dorsally and posteriorly. Subgenital plate subtriangular; with long digitate apical lobe; with four or five macrosetae along lateral margin. Connective Y-shaped; stem very long, 2.4x to 2.7x length of anterior arms. Style preapical lobe large, pronounced, acutely angled, apex rounded; apophysis long, recurved and nearly paralleling preapical lobe, thick at base and gradually attenuated to very thin and sharp apex. Aedeagus in lateral view with base relatively broad, 1/3 to 1/2 height of shaft, dorsally somewhat lightly sclerotized; shaft arising ventrally from base, uniform in width for much of its length, curved throughout its length; gonopore opening subapically on ventral side of shaft; beyond gonopore, extending as a dorsoventrally narrowed portion of shaft; apex reaching beyond aedeagal base; sometimes apex with very short lateral flanges. Aedeagus in caudal view with shaft straight, slightly narrowed ventrally to dorsally; base broadly oval, longer dorsoventrally than transversely. Female ovipositor protruding slightly beyond pygofer apex. Sternite VII posterior margin undulating, forming weakly produced median lobe and two lateral lobes on either side; undulations sometimes very slight, or margin nearly straight.

Morphological notes. The specimen most intensely colored with red is from Zimbabwe (Victoria Falls) ( Fig. 4 ) with strong red coloration on the posterior half of the pronotum, medially along the forewings, spots on either side of the frontoclypeus, on the genae below the eye, on the thoracic pleura, on the legs, and dorsally on the abdomen. Some specimens from Florida were observed with red coloration on the gena ( Fig. 12 ), and/or lightly on the thoracic pleura, legs, and forewing clavus and internal cell enclosed by M and Cu. The dorsal part of the base of the aedeagus is often lightly sclerotized and subject to deformation when removed from the genital capsule. The paratype male imaged here appears to have a slight tear in this area. Depending on the angle of view and the curvature of the female sternite VII, it appears more produced medially in some specimens than shown in Fig. 13 .

Diagnosis. Balclutha jafara can be distinguished from other species in the genus by a combination of characters including the head wider than the pronotum, pygofer without processes, the connective stem nearly 2.5x or more length of anterior arm, the style with preapical lobe large and apex acutely and roundedly angled, the style apophysis long and gradually tapered to very thin and sharply pointed apex, the aedeagus with shaft curved throughout its length, gonopore preapical on ventral side, apical extension beyond gonopore dorsoventrally constricted. Balclutha jafara appears to be very similar to B. viraktamathi Webb & Vilbaste, 1994 described from India. Perhaps the two species will need to be synonymized upon further study, considering the now wider-known distribution of B. jafara . Other species with a similarly long connective are B. bifasciata (Merino) , B. batuensis Knight , B. brevis Lindberg , and B. sujawalensis , from which B. jafara can be distinguished by the shape of the aedeagus, other details of the genitalia, and color pattern.

Material examined. 1♁ paratype: Seychelles Is., Mahe, Beau Vallon, 22.ii.1965, Tams and Nye, B.M. 1966- 72 / PARATYPE, Balclutha jafara Webb, det. M. Webb 1978 / NHMUK 013588847 / Paratype [ BMNH]. 1♀ paratype: Aldabra, South Island, Dune Jean-Louis, 13–20.iii.1968, B. Cogan & A. Hutson / Aldabra Atoll, Royal Society Expedition, 1967–68, B.M. 1968-333 / PARATYPE, Balclutha jafara Webb, Det. M. Webb 1978 / NHMUK 013588848 / Paratype [ BMNH]. 4♁: USA [ USA, new country record]: FLORIDA Palm Beach Co, Belle Glade Everglades R&E Ctr, 3200 E Palm Beach Rd rice paddy, 13-VIII-2021 Donna Larsen Oryza , sativa 26.655 51, -80.62992, FSCA # E2021-4668 [ FSCA, USNM]. 5♀: USA: FLORIDA Palm Beach Co, Okeelanta “Mill Lots” rice paddy, Okeelanta Rd 26.581 38, -80.73592, 13-VIII-2021 Donna Larsen Oryza , sativa FSCA # E2021-4574 [ FSCA, USNM]. 1♁ [intercepted specimen]: From: Colombia [ Colombia, new country record], Port: NY, JFK, ex Mentha sp. , 8.VII.2019 / IMDx _1019 [ USNM]. 1♁ [intercepted specimen]: From: Colombia, Port: NY, JFK, ex Ocimum basilicum , 18.XII.2020 / IMDx _1020 [ USNM]. 1♁ [intercepted specimen]: From: Colombia, Port: FL, Miami, ex Ocimum basilicum , 16.IV.2021 [intercepted specimen]. 1♀ [ BOLD specimen]: BIOUG41827-D06, KEN [ Kenya, new country record]: TU; South Turkwel; Turkana Basin Institute 3.144°N 35.863°E, 457m, 29.Nov– 06.Dec.2014, Dino Martins / Barcode of Life, DNA Voucher Specimen, SampleID: BIOUG41827-D06, ProcessID: GMKTB714–18. 1♁ [ BOLD specimen]: BIOUG41830- C 04, [same data as preceding specimen] / Barcode of Life, DNA Voucher Specimen, SampleID: BIOUG41830- C 04, ProcessID: GMKTB985-18. 1♁ [ BOLD specimen]: BIOUG41838-G11, [same data as preceding] / Barcode of Life, DNA Voucher Specimen, SampleID: BIOUG41838- G11, ProcessID: GMKTB 1800-18. 1 ♁ [ BOLD specimen]: BIOUG41840- C 09, [same data as preceding] / Barcode of Life, DNA Voucher Specimen, SampleID: BIOUG41840- C 09, ProcessID: GMKTB 1940-18. 1 ♁: ZAMBIA [ Zambia, new country record]: Northwestern Prov., ~ 11km SW Mwinilunga, Nkunyi Local Forest, 11°48.809’ S 24°21.953’ E, Hg-vapor light, 4.XI.2007, ZA-04, JN Zahniser / USNMENT01513013 [ USNM]. 1♁: Rhodesia [ Zimbabwe, new country record], Victoria Falls Nat’l Park, IV.3–6.1968, Paul Spangler / USNMENT01513827 [ USNM]. 1♁: *Sudan [ South Sudan, new country record], Yubo, Equatoria / V-12-48, night trap, NMSG #105 / USNMENT01513828 [ USNM]. Suction trap collections (not verbatim): 1♁: USA: FL, Collier Co., Immokalee, SW FL R&E Center, 18.X.2021, Monica Triana, ex short suction trap F-11, LIST# 10252021-5149 [ FSCA]. 1♁: USA: FL, Collier Co., Immokalee, SW FL R&E Center, 24.X.2021, Monica Triana, ex short suction trap F-11, LIST# 11052021-8205 [ FSCA]. 1♁: USA: FL, Collier Co., Immokalee, SW FL R&E Center, 15.XI.2021, Monica Triana, ex short suction trap open field, LIST# 11222-21-7950 [ FSCA]. 2♁: USA: FL, Collier Co., Immokalee, SW FL R&E Center, 13.XII.2021, Monica Triana, ex short suction trap F-11, LIST# 01042022-00048 [ FSCA]. 3♁: USA: FL, Collier Co., Immokalee, 3.I.2022. Monica Triana, ex short suction trap F-11, LIST# 01132022-00293 [ FSCA]. 1♁: USA: FL, Collier Co., Immokalee, 20.XII.2022. Monica Triana, ex short suction trap open field, LIST# 01232023- 00470 [ FSCA]. 1♁: USA: FL, Collier Co., Immokalee, 20.XII.2022. Monica Triana, ex short suction trap F-11, LIST# 01232023-00465 [ FSCA]. 1♁: USA: FL, Palm Beach Co., Belle Glade, Everglades R&E Center, 20.VI.2022, Julien Beuzelin, ex tall suction trap, LIST# 07082022-06246 [ FSCA]. 1♁: USA: FL, Palm Beach Co., Belle Glade, Everglades R&E Center, 24.VII.2023, Julien Beuzelin, ex tall suction trap, LIST# 08102023-08250 [ FSCA].

Additional material. A specimen with a sequence in BOLD (not examined) is recovered in BIN ADS8383 with other B. jafara with the following data: South Africa [ South Africa, new country record], Limpopo, Kruger National Park, Nxanatseni South , Phalaborwa , 23.944°S 31.168°E, 14.V.2018, Col. Verrah, 428 meters [Sample ID BIOUG43382-G01, Sequence ID KMPKA553-18. COI-5 P].

*The verbatim label data are given above. An alternative name for Yubo is Li Yubu (https://www.mindat.org/ feature-371359.html) or Ri Yubu (https://www.geo-locate.org/web/WebGeoref.aspx, https://www.google.com/ maps/) in the state of Western Equatoria, South Sudan.

Identification of specimens. A brief sequence of events for the identification of specimens is given here. In 2021, the Colombia-intercepted specimens and novel FL specimens were determined to be conspecific based on morphology and closely matching COI barcodes (99.85 %). They did not match any known Western Hemisphere ( WH) species morphologically, and the literature on Balclutha from other regions was searched. A close morphological match based on consultation of the literature was made to Balclutha jafara Webb , then known only from the Aldabra and Seychelles Islands ( Webb, 1980). Paratype specimens from BMNH were requested and loaned for examination and DNA sequencing. Morphological examination of the male paratype confirmed a morphological match and partial COI sequences recovered from the paratypes supported species-level identity (97.56%) with Colombia and FL specimens. The COI barcodes of FL and Colombia specimens were searched against the BOLD and GenBank databases and close matches were found in BOLD for several specimens sampled from Kenya and one from South Africa. Voucher specimens were requested and loaned from BOLD, and the identification of B. jafara was confirmed with morphology. Unidentified African specimens of Balclutha at USNM were searched and three were identified as B. jafara .

This combination of specimens shows that B. jafara has a more widespread African distribution than was previously known, and that it has recently become established in the WH, with the earliest known record from an intercepted specimen from Colombia in July, 2019.

Florida records notes. Samples from the FL survey in 2019 recovered no B. jafara . The first known records of B. jafara in Florida are from sweep samples in rice paddies in Palm Beach County in August 2020. In the August 2021 samples, higher numbers were found, and B. jafara was the dominant Balclutha species at four sites ( Fig. 78 ). Several specimens also were collected in the fall and winter of 2021 in short suction traps ( Halbert and Burckhardt, 2020) in Immokalee, Collier Co., Florida. In 2022, a specimen was found in a tall suction trap in Palm Beach Co., Belle Glade, at the Everglades Research and Education Center. Specimens were found again in sweep samples in rice paddies in Palm Beach Co. in August 2022. It was again found in a suction trap sample in July, 2023 at Belle Glade. The increasing observations over recent years is typical for adventive, small Hemiptera . Based on the overall pattern of observations, we suspect that the introduction into Florida is recent.

Balclutha nymphs could not be identified morphologically. Thus, it is uncertain if B. jafara is reproducing on Florida rice. Now that additional identification information is available ( COI barcode data), more research can determine if this species is causing direct damage to the crop or transmitting plant pathogens.

Ecology and host plants. Like other species of Balclutha , B. jafara is a grass feeder. The records in Florida are from commercial rice paddies. Balclutha jafara infestations were not associated with obvious symptoms of stress potentially caused by leafhoppers. Although the specimens from Colombia were intercepted on shipments of basil and mint, these should not be considered host records because the specimens could have become associated with these products from surrounding vegetation.

In Kenya, the habitat at the Turkana site is described as follows: Turkana Basin Institute Malaise Trap is within South Turkwel campus at Nachekichok, Turkana County, Kenya. Open woodland habitat dominated by trees Vachellia tortilis (Forssk.) Galasso & Banfi ( Fabaceae ) and V. reficiens (Wawra & Peyr.) Kyal. & Boatwr. , and shrubs including Salvadora persica L. ( Salvadoraceae ), Combretum rotundifolium Rich. , and perennial groundcover primarily Indigofera spinosa (Forssk.) ( Fabaceae ), I. circinella Baker f. , Heliotropium sp. ( Boraginaceae ), Aristida spp. ( Poaceae ) and Dactyloctenium sp. ( Poaceae ). Hot and arid climate, semi-desert, rainfall ca. 250mm /year. Mean temperature 23-35°C ( Martins, 2015; Miller et al., 2014).

All five rice paddies where B. jafara was collected in August 2021 were surrounded by sugarcane.Weedy grasses in field margins at the Everglades Research and Education Center included bermudagrass- Cynodon dactylon (L.) Pers., goosegrass- Eleusine indica (L.) Gaertn., crowfootgrass- Dactyloctenium aegyptium (L.) Willd., crabgrass- Digitaria sp. , and elephant grass- Pennisetum purpureum Schumach. Weedy grasses in margins of the other four locations also included Columbus grass- Sorghum almum Parodi , which was relatively abundant at the “Sem Chi” site. However, elephant grass was absent at the “Triangle”, “Resmondo” and “Mill Lot S” sites. In August 2021, when the highest numbers of B. jafara were found in rice, concurrent samples of adjacent sugarcane failed to yield any B. jafara , suggesting that sugarcane was not a preferred host.

Figures

FIGURE 77. Mainland Africa and Indian Oceanic Island records of B. jafara and B. sujawalensis.

FIGURE 78. Map of the Everglades Agricultural Area showing rice paddy sample locations and numbers of Balclutha species collected in the August, 2021 sampling period. Map by Kate Love and Alicia Lawrence, FDACS, DPI.

FIGURES 1–10. Balclutha jafara habitus. (1) male, Colombia, dorsal, IMDx_1020; (2) male paratype, Seychelles, dorsal, NHMUK 013588847; (3) male, Colombia, IMDx_1019; (4) male, Zimbabwe, dorsal, USNMENT01513827; (5) female paratype, Aldabra, dorsal, NHMUK 013588848; (6) male, South Sudan, dorsal, USNMENT01513828; (7) male, Colombia, dorsal, JNZ_AA0474; (8) same, ventral; (9) male, Colombia, lateral, IMDx_1020; (10) male, Colombia, lateral, JNZ_AA0474. Figs. 7–8, 10: images taken of specimen immersed in ethanol.

FIGURES 11–13. Balclutha jafara. (11) face, anterior view, male, South Sudan, USNMENT01513828; (12) face, anterolateral view, male, USA: FL: Belle Glade, JNZ_AA0134; (13) sternite VII, female paratype, Aldabra, NHMUK 013588848.

FIGURES 14–21. Balclutha jafara male genitalia. (14–16, Colombia, IMDx_1019): (14) connective and styles, ventral; (15) pygofer, lateral; (16) valve and subgenital plate, ventral. (17) connective, style, and partial base of aedeagus, ventral, paratype, Seychelles, NHMUK 013588847; (18–19, Zimbabwe, USNMENT01513827): (18) genital capsule, lateral; (19) genital capsule, ventral. (20–21, Kenya, BIOUG41840-C09): (20) genital capsule, lateral; (21) genital capsule, ventral.

FIGURES 22–27. Balclutha jafara aedeagus. (22–26, lateral; 27, caudal): (22) Colombia, IMDx_1020; (23) paratype, Seychelles, NHMUK 013588847; (24) USA: FL: Belle Glade, JNZ_AA0114; (25) Zimbabwe, USNMENT01513827; (26–27) South Sudan, USNMENT01513828.